The use of the chorioallantoic membrane as an experimental model for studying markers of endometrial receptivity
https://doi.org/10.59598/ME-2305-6045-2024-113-4-43-52
Abstract
The article presents a review of articles aimed at summarizing the results of studies using the choriollantoic membrane (СAM) to study markers and mechanisms of endometrial receptivity and angiogenesis. Considering these studies together clarifies the complex regulatory networks involved in vascular development and endometrial susceptibility. Understanding the intricacies of angiogenesis and endometrial susceptibility is crucial in reproductive medicine and infertility treatment. The chorioallantoic membrane (CAM) and its analogues, the angiogenic model derived from stroma (CAM), offer valuable platforms for such research. A comprehensive search of scientific literature databases was conducted to identify relevant studies using CAM. Studies using CAM have provided insight into markers of endometrial susceptibility, shedding light on structural changes associated with vascular development. Similarly, studies using CAM have provided valuable information on pinopods and other markers indicating endometrial susceptibility, indicating potential clinical applications in reproductive medicine. Together, these studies contribute to a deeper understanding of the cellular and molecular mechanisms of endometrial regulation. They emphasize the role of various factors, including growth factors, cytokines, and signaling pathways, in inducing endometrial angiogenesis and modulating its susceptibility. Such findings can serve as a basis for the development of new diagnostic and therapeutic strategies in reproductive medicine.
About the Authors
A. B. MussayepovaKazakhstan
Assel Berikovna Mussayepova – doctoral student of 1st year of study
100008, Karaganda, Gogol street, 40
Y. G. Turdybekova
Kazakhstan
100008, Karaganda, Gogol street, 40
B. B. Rakhimova
Kazakhstan
100008, Karaganda, Gogol street, 40
I. L. Kopobaeva
Kazakhstan
100008, Karaganda, Gogol street, 40
References
1. Kazahstanskij Institut obshhestvennogo razvitija. Nacional'nyj doklad «Kazahstanskie sem'i-2022» //https://ru.kipd.kz/article/kazakhstanskiesemi-2022-natsionalnyy-doklad (data obrashhenija: 12.03.2024)
2. Chertok V. M. Jendoteliozavisimaja reguljacija angiogeneza /V. M. Chertok, A. G. Chertok, V. G. Zenkina //Citologija. – 2017. – T. 59, №4. – S. 243-258.
3. Abdelazim I. A. Miscarriage definitions, causes and management: review of literature //ARC J. Gynecol. Obstet. – 2017. – V. 2, №3. – P. 20-31.
4. Aoyama K. Risk prediction models for maternal mortality: a systematic review and metaanalysis //PLoS One. – 2018. – V. 13 (12). – e0208563.
5. Beal J. R. Role of Endometrial Extracellular Vesicles in Mediating Cell-to-Cell Communication in the Uterus: A Review //Cells. – 2023. – V. 12 (22). – P. 2584.
6. Boretto M. Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability // Development. – 2017. – V. 144 (10). – P. 1775-1786.
7. Bortoletto P. Miscarriage syndrome: linking early pregnancy loss to obstetric and age-related disorders //EBioMedicine. – 2022. – V. 81. – 104134.
8. Brooks P. C. Requirement of vascular integrin αvβ3 for angiogenesis /P. C. Brooks, R. A. F. Clark, D. A. Cheresh //Science. – 1994. – V. 264 (5158). – P. 569-571.
9. Chakhtoura N. Importance of research in reducing maternal morbidity and mortality rates // American Journal of Obstetrics & Gynecology. – 2019. – V. 221 (3). – P. 179-182.
10. Check J. H. Very thin endometria in the late proliferative phase is more associated with poor pregnancy rates following controlled ovarian hyperstimulation than graduated estradiol regimens used for frozen embryo transfer //Fertility and Sterility. – 2014. – V. 101 (2). – e21.
11. Chen X. Physiological and pathological angiogenesis in endometrium at the time of embryo implantation //American Journal of Reproductive Immunology. – 2017. – V. 78 (2). – e12693.
12. Chioran D. Nicotine Exerts Cytotoxic Effects in a Panel of Healthy Cell Lines and Strong Irritating Potential on Blood Vessels //International Journal of Environmental Research and Public Health. – 2022. – V. 19 (14). – P. 8881.
13. Ciavattini A. Uterine fibroids: pathogenesis and interactions with endometrium and endomyometrial junction //Obstetrics and gynecology international. – 2013. – V. 2013. – 173184.
14. Dawood F. Investigation of recurrent miscarriage /F. Dawood, R. G. Farquharson, M. D. Stephenson //Early Pregnancy. – 2010. – V. 331. – P. 59-66.
15. Dix E. Successful pregnancies following embryo transfer despite very thin late proliferative endometrium /E. Dix, J. H. Check //Clinical and experimental obstetrics & gynecology. – 2010. – V. 37 (1). – P. 15-16.
16. Dugas C. Miscarriage /C. Dugas, V. H. Slane //Treasure Island, FL: StatPearls Publishing //https:// www.ncbi.nlm.nih.gov/books/NBK532992 (accessed: March 7, 2024).
17. Ecay T. W. Expression of calbindin-D28K by yolk sac and chorioallantoic membranes of the corn snake, Elaphe guttata /T. W. Ecay, J. R. Stewart, D. G. Blackburn //Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. – 2004. – V. 302 (6). – P. 517-525.
18. Edwards A. K. Expression of angiogenic basic fibroblast growth factor, platelet derived growth factor, thrombospondin-1 and their receptors at the porcine maternal-fetal interface //Reproductive Biology and Endocrinology. – 2011. – V. 9. – P. 1-11.
19. Ellis P. E. Molecular characteristics and risk factors in endometrial cancer: what are the treatment and preventative strategies? /P. E. Ellis, S. Ghaem-Maghami //International Journal of Gynecologic Cancer. – 2010. – V. 20 (7). – P. 1207-1216.
20. Evans J. Fertile ground: human endometrial programming and lessons in health and disease // Nature Reviews Endocrinology. – 2016. – V. 12 (11). – P. 654-667.
21. Evans J. In vitro human implantation model reveals a role for endometrial extracellular vesicles in embryo implantation: reprogramming the cellular and secreted proteome landscapes for bidirectional fetalmaternal communication //Proteomics. – 2019. – V. 19 (23). – 1800423.
22. Giakoumelou S. The role of infection in miscarriage //Human reproduction update. – 2016. – V. 22 (1). – P. 116-133.
23. Giri S. K. Thickened endometrium: when to intervene? A clinical conundrum /S. K. Giri, B. L. Nayak, J. Mohapatra //The Journal of Obstetrics and Gynecology of India. – 2021. – V. 71 (3). – P. 216-225.
24. Gray C. A. Developmental biology of uterine glands //Biology of reproduction. – 2001. – V. 65 (5). – P. 1311-1323.
25. Hardy K. 1st trimester miscarriage: four decades of study /K. Hardy, P. J. Hardy //Translational pediatrics. – 2015. – V. 4 (2). – P. 189.
26. Hviid S. M. Are different markers of endometrial receptivity telling us different things about endometrial function? //American Journal of Reproductive Immunology. – 2020. – V. 84 (6). – e13323.
27. Javan-Jaafari-Bojnourdi T. The effect of alcoholic extract of Persian gulf chiton (lamyi) shell on angiogenesis in chick chorioallantoic membrane /T. Javan-Jaafari-Bojnourdi, J. Baharara //Zahedan Journal of Research in Medical Sciences. – 2015. – V. 17 (3). – e24474.
28. Kolanska K. Role of miRNAs in normal endometrium and in endometrial disorders: comprehensive review //Journal of Clinical Medicine. – 2021. – V. 10 (16). – P. 3457.
29. Larsen E. C. New insights into mechanisms behind miscarriage //BMC medicine. – 2013. – V. 11. – P. 1-10.
30. Liu L. The impact of chronic endometritis on endometrial fibrosis and reproductive prognosis in patients with moderate and severe intrauterine adhesions: a prospective cohort study //Fertility and sterility. – 2019. – V. 111 (5). – P. 1002-1010.
31. Liu M. Use of animal models for the imaging and quantification of angiogenesis /M. Liu, S. Xie, J. Zhou //Experimental animals. – 2018. – V. 67 (1). – P. 1-6.
32. Makrigiannakis A. Approaches to improve endometrial receptivity in case of repeated implantation failures /A. Makrigiannakis, F. Makrygiannakis, T. Vrekoussis //Frontiers in cell and developmental biology. – 2021. – V. 9. – P. 613277.
33. Matzuk M. M. The biology of infertility: research advances and clinical challenges /M. M. Matzuk, D. J. Lamb //Nature medicine. – 2008. – V. 14 (11). – P. 1197-1213.
34. Maurya V. K. Illuminating the «Black Box» of progesterone-dependent embryo implantation using engineered mice /V. K. Maurya, F. J. DeMayo, J. P. Lydon //Frontiers in Cell and Developmental Biology. – 2021. – V. 9. – P. 640907.
35. Myatt S. S. Definition of microRNAs that repress expression of the tumor suppressor gene FOXO1 in endometrial cancer //Cancer research. – 2010. – V. 70 (1). – P. 367-377.
36. Newbatt E. Ectopic pregnancy and miscarriage: summary of NICE guidance //BMJ. – 2012. – V. 345. – e8136
37. Nikas G. Pinopodes as markers of endometrial receptivity in clinical practice //Human Reproduction. – 1999. – V. 14, Suppl. 2. – P. 99-106.
38. Nowak-Sliwinska P. et al. Oncofoetal insulin receptor isoform A marks the tumour endothelium; an underestimated pathway during tumour angiogenesis and angiostatic treatment //British journal of cancer. – 2019. – V. 120 (2). – P. 218-228.
39. Nowak-Sliwinska P. The chicken chorioallantoic membrane model in biology, medicine and bioengineering /P. Nowak-Sliwinska, T. Segura, M. L. Iruela-Arispe //Angiogenesis. – 2014. – V. 17. – P. 779-804.
40. Okada H. Decidualization of the human endometrium /H. Okada, T. Tsuzuki, H. Murata // Reproductive medicine and biology. – 2018. – V. 17 (3). – P. 220-227.
41. Ordi J. Endometrial pinopode and αvβ3 integrin expression is not impaired in infertile patients with endometriosis //Journal of assisted reproduction and genetics. – 2003. – V. 20. – P. 465-473.
42. Pathuri G. Solid phase synthesis and biological evaluation of probestin as an angiogenesis inhibitor //Bioorganic & medicinal chemistry letters. – 2013. – V. 23 (12). – P. 3561-3564.
43. Prost A. Women's groups practising participatory learning and action to improve maternal and newborn health in low-resource settings: a systematic review and meta-analysis //The Lancet. – 2013. – V. 381 (9879). – P. 1736-1746.
44. Quinn C. E. Pinopodes: a questionable role in endometrial receptivity /C. E. Quinn, R. F. Casper // Human reproduction update. – 2009. – V. 15 (2). – P. 229-236.
45. Rackow B. W. Endometrial polyps affect uterine receptivity /B. W. Rackow, E. Jorgensen, H. S. Taylor //Fertility and sterility. – 2011. – V. 95 (8). – P. 2690-2692.
46. Rackow B. W. Submucosal uterine leiomyomas have a global effect on molecular determinants of endometrial receptivity /B. W. Rackow, H. S. Taylor //Fertility and sterility. – 2010. – V. 93 (6). – P. 2027-2034.
47. Ramakrishnan U. Effect of women's nutrition before and during early pregnancy on maternal and infant outcomes: a systematic review //Paediatric and perinatal epidemiology. – 2012. – V. 26. – P. 285-301.
48. Ribatti D. Chorioallantoic membrane capillary bed: a useful target for studying angiogenesis and anti-angiogenesis in vivo //The Anatomical Record: An Official Publication of the American Association of Anatomists. – 2001. – V. 264 (4). – P. 317-324.
49. Riley I. D. Monitoring progress in reducing maternal mortality using verbal autopsy methods in vital registration systems: what can we conclude about specific causes of maternal death? //BMC medicine. – 2019. – V. 17. – P. 1-4.
50. Rogers P. A. W. Endometrial angiogenesis, vascular maturation, and lymphangiogenesis // Reproductive Sciences. – 2009. – V. 16 (2). – P. 147-151.
51. Schöniger S. The healthy and diseased equine endometrium: A review of morphological features and molecular analyses /S. Schöniger, H. A. Schoon //Animals. – 2020. – V. 10 (4). – P. 625.
52. Staton C. A. Current methods for assaying angiogenesis in vitro and in vivo //International journal of experimental pathology. – 2004. – V. 85 (5). – P. 233-248.
53. Sudoma I. Optimization of cryocycles by using pinopode detection in patients with multiple implantation failure: preliminary report /I. Sudoma, Goncharova Y., Zukin V. //Reproductive BioMedicine Online. – 2011. – V. 22 (6). – P. 590-596.
54. Sutaji Z. A systematic review and integrated bioinformatic analysis of candidate genes and pathways in the endometrium of patients with polycystic ovary syndrome during the implantation window //Frontiers in Endocrinology. – 2022. – V. 13. – P. 900767.
55. Tan W. Relationship between macrophages in mouse uteri and angiogenesis in endometrium during the peri-implantation period //Theriogenology. – 2014. – V. 82 (7). – P. 1021-1027.
56. Tan O. Expression and activation of the membrane-cytoskeleton protein ezrin during the normal endometrial cycle //Fertility and sterility. – 2012. – V. 97 (1). – P. 192-199.
57. Tayade C. Lymphocyte contributions to altered endometrial angiogenesis during early and midgestation fetal loss //Journal of Leucocyte Biology. – 2007. – V. 82 (4). – P. 877-886.
58. Verhoelst E. The effect of early prenatal hypercapnia on the vascular network in the chorioallantoic membrane of the chicken embryo // Biotechnology progress. – 2011. – V. 27 (2). – P. 562-570.
59. Wilson R. Thyroid antibody titer and avidity in patients with recurrent miscarriage //Fertility and sterility. – 1999. – V. 71 (3). – P. 558-561.
60. Zacharakis N. Methylene blue inhibits angiogenesis in chick chorioallontic membrane through a nitric oxide-independent mechanism // Journal of Cellular and Molecular Medicine. – 2006. – V. 10 (2). – P. 493-498.
61. Zhao X. Deciphering the endometrial immune landscape of RIF during the window of implantation from cellular senescence by integrated bioinformatics analysis and machine learning //Frontiers in Immunology. – 2022. – V. 13. – P. 952708.
Review
For citations:
Mussayepova A.B., Turdybekova Y.G., Rakhimova B.B., Kopobaeva I.L. The use of the chorioallantoic membrane as an experimental model for studying markers of endometrial receptivity. Medicine and ecology. 2024;(4):43-52. (In Russ.) https://doi.org/10.59598/ME-2305-6045-2024-113-4-43-52